TY - JOUR
T1 - Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
AU - Inagaki, Hideo
AU - Miyamoto, Koji
AU - Ando, Noriko
AU - Murakami, Kohei
AU - Sugisawa, Koki
AU - Morita, Shion
AU - Yumoto, Emi
AU - Teruya, Miyu
AU - Uchida, Kenichi
AU - Kato, Nobuki
AU - Kaji, Takuya
AU - Takaoka, Yousuke
AU - Hojo, Yuko
AU - Shinya, Tomonori
AU - Galis, Ivan
AU - Nozawa, Akira
AU - Sawasaki, Tatsuya
AU - Nojiri, Hideaki
AU - Ueda, Minoru
AU - Okada, Kazunori
N1 - Funding Information:
We would like to thank Hisakazu Yamane (The University of Tokyo) for his advice; Peter Nick and Michael Riemann for providing an expression vector for OsAOC; Ryosuke Sato (Teikyo University) for providing the SLiCE; and Kenichiro Hayashi (Okayama University of Science) for providing C. plumiforme plants. We would also like to thank Izumi C. Mori and Takakazu Matsuura (Okayama University) for their insights and technical assistance in [2H5]-dn-OPDA synthesis. Funding. This work was supported by JSPS KAKENHI (Grant Numbers JP18K14399 to KMi; JP20H02922 to KO; JP17H06407, JP18KK0162, and JP20H00402 to MU; JP18H02101 and JP19H05283 to YT), JSPS A3 Foresight Program to MU, Japan-Austria Research Cooperative Program between JSPS and FWF (Grant Number JPJSBP120202002) to KO, and the Joint Usage/Research Center, Institute of Plant Science and Resources, Okayama University.
Funding Information:
This work was supported by JSPS KAKENHI (Grant Numbers JP18K14399 to KMi; JP20H02922 to KO; JP17H06407, JP18KK0162, and JP20H00402 to MU; JP18H02101 and JP19H05283 to YT), JSPS A3 Foresight Program to MU, Japan-Austria Research Cooperative Program between JSPS and FWF (Grant Number JPJSBP120202002) to KO, and the Joint Usage/Research Center, Institute of Plant Science and Resources, Okayama University.
Publisher Copyright:
© Copyright © 2021 Inagaki, Miyamoto, Ando, Murakami, Sugisawa, Morita, Yumoto, Teruya, Uchida, Kato, Kaji, Takaoka, Hojo, Shinya, Galis, Nozawa, Sawasaki, Nojiri, Ueda and Okada.
PY - 2021/5/31
Y1 - 2021/5/31
N2 - Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA). In the presence of JA-Ile, the COI1 receptor physically interacts with JAZ repressors, leading to their degradation, resulting in the transcription of JA-responsive genes by MYC transcription factors. Although the biosynthesis of JA-Ile is conserved in vascular plants, it is not recognized by COI1 in bryophytes and is not biologically active. In the liverwort Marchantia polymorpha, dinor-OPDA (dn-OPDA), a homolog of OPDA with two fewer carbons, and its isomer dn-iso-OPDA accumulate after wounding and are recognized by COI1 to activate downstream signaling. The moss Calohypnum plumiforme produces the antimicrobial-specialized metabolites, momilactones. It has been reported that JA and JA-Ile are not detected in C. plumiforme and that OPDA, but not JA, can induce momilactone accumulation and the expression of these biosynthetic genes, suggesting that OPDA or its derivative is a biologically active molecule in C. plumiforme that induces chemical defense. In the present study, we investigated the biological functions of OPDA and its derivatives in C. plumiforme. Searching for the components potentially involving oxylipin signaling from transcriptomic and genomic data revealed that two COI1, three JAZ, and two MYC genes were present. Quantification analyses revealed that OPDA and its isomer iso-OPDA accumulated in larger amounts than dn-OPDA and dn-iso-OPDA after wounding. Moreover, exogenously applied OPDA, dn-OPDA, or dn-iso-OPDA induced the transcription of JAZ genes. These results imply that OPDA, dn-OPDA, and/or their isomers potentially act as biologically active molecules to induce the signaling downstream of COI1-JAZ. Furthermore, co-immunoprecipitation analysis showed the physical interaction between JAZs and MYCs, indicating the functional conservation of JAZs in C. plumiforme with other plants. These results suggest that COI1-JAZ-MYC mediated signaling is conserved and functional in C. plumiforme.
AB - Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA). In the presence of JA-Ile, the COI1 receptor physically interacts with JAZ repressors, leading to their degradation, resulting in the transcription of JA-responsive genes by MYC transcription factors. Although the biosynthesis of JA-Ile is conserved in vascular plants, it is not recognized by COI1 in bryophytes and is not biologically active. In the liverwort Marchantia polymorpha, dinor-OPDA (dn-OPDA), a homolog of OPDA with two fewer carbons, and its isomer dn-iso-OPDA accumulate after wounding and are recognized by COI1 to activate downstream signaling. The moss Calohypnum plumiforme produces the antimicrobial-specialized metabolites, momilactones. It has been reported that JA and JA-Ile are not detected in C. plumiforme and that OPDA, but not JA, can induce momilactone accumulation and the expression of these biosynthetic genes, suggesting that OPDA or its derivative is a biologically active molecule in C. plumiforme that induces chemical defense. In the present study, we investigated the biological functions of OPDA and its derivatives in C. plumiforme. Searching for the components potentially involving oxylipin signaling from transcriptomic and genomic data revealed that two COI1, three JAZ, and two MYC genes were present. Quantification analyses revealed that OPDA and its isomer iso-OPDA accumulated in larger amounts than dn-OPDA and dn-iso-OPDA after wounding. Moreover, exogenously applied OPDA, dn-OPDA, or dn-iso-OPDA induced the transcription of JAZ genes. These results imply that OPDA, dn-OPDA, and/or their isomers potentially act as biologically active molecules to induce the signaling downstream of COI1-JAZ. Furthermore, co-immunoprecipitation analysis showed the physical interaction between JAZs and MYCs, indicating the functional conservation of JAZs in C. plumiforme with other plants. These results suggest that COI1-JAZ-MYC mediated signaling is conserved and functional in C. plumiforme.
KW - 12-oxo-phytodienoic acid
KW - Calohypnum plumiforme
KW - moss
KW - oxylipin
KW - plant hormone
UR - http://www.scopus.com/inward/record.url?scp=85107836460&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85107836460&partnerID=8YFLogxK
U2 - 10.3389/fpls.2021.688565
DO - 10.3389/fpls.2021.688565
M3 - Article
AN - SCOPUS:85107836460
SN - 1664-462X
VL - 12
JO - Frontiers in Plant Science
JF - Frontiers in Plant Science
M1 - 688565
ER -